Effects of the fusion design and immunization route on the immunogenicity of Ag85A-Mtb32 in adenoviral vectored tuberculosis vaccine

References

• Organization WH. Global Tuberculosis Report 2013. http://www.who.int/tb/publications/global_report/en/2013.
   Google Scholar
• Montagnani C, Chiappini E, Galli L, de Martino M. Vaccine against tuberculosis: what's new? BMC Infect Dis 2014; 14 Suppl 1:S2; PMID:24564340; http://dx.doi.org/10.1186/1471-2334-14-S1-S2
   PubMed Web of Science ®Google Scholar
• Mittrucker HW, Steinhoff U, Kohler A, Krause M, Lazar D, Mex P, Miekley D, Kaufmann SH. Poor correlation between BCG vaccination-induced T cell responses and protection against tuberculosis. P Natl Acad Sci USA 2007; 104:12434-9; http://dx.doi.org/10.1073/pnas.0703510104
   PubMed Web of Science ®Google Scholar
• Smaill F, Jeyanathan M, Smieja M, Medina MF, Thanthrige-Don N, Zganiacz A, Yin C, Heriazon A, Damjanovic D, Puri L, et al. A Human Type 5 Adenovirus-Based Tuberculosis Vaccine Induces Robust T Cell Responses in Humans Despite Preexisting Anti-Adenovirus Immunity. Sci Transl Med 2013; 5:205ra134
   PubMed Web of Science ®Google Scholar
• Abel B, Tameris M, Mansoor N, Gelderbloem S, Hughes J, Abrahams D, Makhethe L, Erasmus M, de Kock M, van der Merwe L, et al. The novel tuberculosis vaccine, AERAS-402, induces robust and polyfunctional CD4+ and CD8+ T cells in adults. Am J Respir Crit Care Med 2010; 181:1407-17; PMID:20167847; http://dx.doi.org/10.1164/rccm.200910-1484OC
   PubMed Web of Science ®Google Scholar
• Scriba TJ, Tameris M, Mansoor N, Smit E, van der Merwe L, Isaacs F, Keyser A, Moyo S, Brittain N, Lawrie A, et al. Modified vaccinia Ankara-expressing Ag85A, a novel tuberculosis vaccine, is safe in adolescents and children, and induces polyfunctional CD4+ T cells. Eur J Immunol 2010; 40:279-90; PMID:20017188; http://dx.doi.org/10.1002/eji.200939754
   PubMed Web of Science ®Google Scholar
• Mu J, Jeyanathan M, Small CL, Zhang X, Roediger E, Feng X, Chong D, Gauldie J, Xing Z. Immunization with a bivalent adenovirus-vectored tuberculosis vaccine provides markedly improved protection over its monovalent counterpart against pulmonary tuberculosis. Mol Ther 2009; 17:1093-100; PMID:19319120; http://dx.doi.org/10.1038/mt.2009.60
   PubMed Web of Science ®Google Scholar
• Tameris MD, Hatherill M, Landry BS, Scriba TJ, Snowden MA, Lockhart S, Shea JE, McClain JB, Hussey GD, Hanekom WA, et al. Safety and efficacy of MVA85A, a new tuberculosis vaccine, in infants previously vaccinated with BCG: a randomised, placebo-controlled phase 2b trial. Lancet 2013; 381:1021-8; http://dx.doi.org/10.1016/S0140-6736(13)60177-4
   PubMed Web of Science ®Google Scholar
• Havenga M, Vogels R, Zuijdgeest D, Radosevic K, Mueller S, Sieuwerts M, Weichold F, Damen I, Kaspers J, Lemckert A, et al. Novel replication-incompetent adenoviral B-group vectors: high vector stability and yield in PER.C6 cells. J Gen Virol 2006; 87:2135-43; PMID:16847108; http://dx.doi.org/10.1099/vir.0.81956-0
   PubMed Web of Science ®Google Scholar
• Mir FA, Kaufmann SH, Eddine AN. A multicistronic DNA vaccine induces significant protection against tuberculosis in mice and offers flexibility in the expressed antigen repertoire. Clin Vaccine Immunol 2009; 16:1467-75; PMID:19656992; http://dx.doi.org/10.1128/CVI.00237-09
   PubMed Web of Science ®Google Scholar
• Yuan W, Dong N, Zhang L, Liu J, Lin S, Xiang Z, Qiao H, Tong W, Qin C. Immunogenicity and protective efficacy of a tuberculosis DNA vaccine expressing a fusion protein of Ag85B-Esat6-HspX in mice. Vaccine 2012; 30:2490-7; PMID:21704108; http://dx.doi.org/10.1016/j.vaccine.2011.06.029
   PubMed Web of Science ®Google Scholar
• Perez de Val B, Vidal E, Villarreal-Ramos B, Gilbert SC, Andaluz A, Moll X, Martín M, Nofrarías M, McShane H, Vordermeier HM, et al. A multi-antigenic adenoviral-vectored vaccine improves BCG-induced protection of goats against pulmonary tuberculosis infection and prevents disease progression. PloS one 2013; 8:e81317; PMID:24278420; http://dx.doi.org/10.1371/journal.pone.0081317
   PubMed Web of Science ®Google Scholar
• Whelan A, Court P, Xing Z, Clifford D, Hogarth PJ, Vordermeier M, Villarreal-Ramos B. Immunogenicity comparison of the intradermal or endobronchial boosting of BCG vaccinates with Ad5-85A. Vaccine 2012; 30:6294-300; PMID:22885013; http://dx.doi.org/10.1016/j.vaccine.2012.07.086
   PubMed Web of Science ®Google Scholar
• McCluskie MJ, Brazolot Millan CL, Gramzinski RA, Robinson HL, Santoro JC, Fuller JT, Widera G, Haynes JR, Purcell RH, Davis HL. Route and method of delivery of DNA vaccine influence immune responses in mice and non-human primates. Mol Med 1999; 5:287-300; PMID:10390545; http://dx.doi.org/10.1007/s0089490050287
   PubMed Web of Science ®Google Scholar
• Wang J, Thorson L, Stokes RW, Santosuosso M, Huygen K, Zganiacz A, Hitt M, Xing Z. Single mucosal, but not parenteral, immunization with recombinant adenoviral-based vaccine provides potent protection from pulmonary tuberculosis. J Immunol 2004; 173:6357-65; http://dx.doi.org/10.4049/jimmunol.173.10.6357
   PubMed Web of Science ®Google Scholar
• Xing Z, McFarland CT, Sallenave JM, Izzo A, Wang J, McMurray DN. Intranasal mucosal boosting with an adenovirus-vectored vaccine markedly enhances the protection of BCG-primed guinea pigs against pulmonary tuberculosis. PloS one 2009; 4:e5856; PMID:19516906; http://dx.doi.org/10.1371/journal.pone.0005856
   PubMed Web of Science ®Google Scholar
• Forbes EK, Sander C, Ronan EO, McShane H, Hill AV, Beverley PC, Tchilian EZ. Multifunctional, high-level cytokine-producing Th1 cells in the lung, but not spleen, correlate with protection against Mycobacterium tuberculosis aerosol challenge in mice. J Immunol 2008; 181:4955-64; http://dx.doi.org/10.4049/jimmunol.181.7.4955
   PubMed Web of Science ®Google Scholar
• Santosuosso M, Zhang X, McCormick S, Wang J, Hitt M, Xing Z. Mechanisms of mucosal and parenteral tuberculosis vaccinations: adenoviral-based mucosal immunization preferentially elicits sustained accumulation of immune protective CD4 and CD8 T cells within the airway lumen. J Immunol 2005; 174:7986-94; http://dx.doi.org/10.4049/jimmunol.174.12.7986
   PubMed Web of Science ®Google Scholar
• Santosuosso M, McCormick S, Roediger E, Zhang X, Zganiacz A, Lichty BD, Xing Z. Mucosal luminal manipulation of T cell geography switches on protective efficacy by otherwise ineffective parenteral genetic immunization. J Immunol 2007; 178:2387-95; http://dx.doi.org/10.4049/jimmunol.178.4.2387
   PubMed Web of Science ®Google Scholar
• Vordermeier HM, Villarreal-Ramos B, Cockle PJ, McAulay M, Rhodes SG, Thacker T, Gilbert SC, McShane H, Hill AV, Xing Z, et al. Viral booster vaccines improve Mycobacterium bovis BCG-induced protection against bovine tuberculosis. Infect Immun 2009; 77:3364-73; PMID:19487476; http://dx.doi.org/10.1128/IAI.00287-09
   PubMed Web of Science ®Google Scholar
• Ahn SS, Jeon BY, Kim KS, Kwack JY, Lee EG, Park KS, Sung YC, Cho SN. Mtb32 is a promising tuberculosis antigen for DNA vaccination in pre- and post-exposure mouse models. Gene Ther 2012; 19:570-5; PMID:21956689; http://dx.doi.org/10.1038/gt.2011.140
   PubMed Web of Science ®Google Scholar
• Cooper AM, Mayer-Barber KD, Sher A. Role of innate cytokines in mycobacterial infection. Mucosal Immunol 2011; 4:252-60; PMID:21430655; http://dx.doi.org/10.1038/mi.2011.13
   PubMed Web of Science ®Google Scholar
• Redford PS, Boonstra A, Read S, Pitt J, Graham C, Stavropoulos E, Bancroft GJ, O'Garra A. Enhanced protection to Mycobacterium tuberculosis infection in IL-10-deficient mice is accompanied by early and enhanced Th1 responses in the lung. Eur J Immunol 2010; 40:2200-10; PMID:20518032; http://dx.doi.org/10.1002/eji.201040433
   PubMed Web of Science ®Google Scholar
• Derrick SC, Yabe IM, Yang A, Morris SL. Vaccine-induced anti-tuberculosis protective immunity in mice correlates with the magnitude and quality of multifunctional CD4 T cells. Vaccine 2011; 29:2902-9; PMID:21338678; http://dx.doi.org/10.1016/j.vaccine.2011.02.010
   PubMed Web of Science ®Google Scholar
• Caccamo N, Meraviglia S, La Mendola C, Guggino G, Dieli F, Salerno A. Phenotypical and functional analysis of memory and effector human CD8 T cells specific for mycobacterial antigens. J Immunol 2006; 177:1780-5; http://dx.doi.org/10.4049/jimmunol.177.3.1780
   PubMed Web of Science ®Google Scholar
• Caccamo N, Guggino G, Meraviglia S, Gelsomino G, Di Carlo P, Titone L, Bocchino M, Galati D, Matarese A, Nouta J, et al. Analysis of Mycobacterium tuberculosis-specific CD8 T-cells in patients with active tuberculosis and in individuals with latent infection. PloS one 2009; 4:e5528; PMID:19436760; http://dx.doi.org/10.1371/journal.pone.0005528
   PubMed Web of Science ®Google Scholar
• Cid-Arregui A, Juarez V, zur Hausen H. A synthetic E7 gene of human papillomavirus type 16 that yields enhanced expression of the protein in mammalian cells and is useful for DNA immunization studies. J Virol 2003; 77:4928-37; PMID:12663798; http://dx.doi.org/10.1128/JVI.77.8.4928-4937.2003
   PubMed Web of Science ®Google Scholar
• Ramakrishna L, Anand KK, Mohankumar KM, Ranga U. Codon optimization of the tat antigen of human immunodeficiency virus type 1 generates strong immune responses in mice following genetic immunization. J Virol 2004; 78:9174-89; PMID:15308713; http://dx.doi.org/10.1128/JVI.78.17.9174-9189.2004
   PubMed Web of Science ®Google Scholar
• Ko HJ, Ko SY, Kim YJ, Lee EG, Cho SN, Kang CY. Optimization of codon usage enhances the immunogenicity of a DNA vaccine encoding mycobacterial antigen Ag85B. Infect Immun 2005; 73:5666-74; PMID:16113284; http://dx.doi.org/10.1128/IAI.73.9.5666-5674.2005
   PubMed Web of Science ®Google Scholar
• Wen B, Deng Y, Guan J, Yan W, Wang Y, Tan W, Gao J. Signal peptide replacements enhance expression and secretion of hepatitis C virus envelope glycoproteins. Acta biochimica et biophysica Sinica 2011; 43:96-102; PMID:21196448; http://dx.doi.org/10.1093/abbs/gmq117
   PubMed Web of Science ®Google Scholar
• de Felipe P, Luke GA, Brown JD, Ryan MD. Inhibition of 2A-mediated ‘cleavage’ of certain artificial polyproteins bearing N-terminal signal sequences. Biotechnol J 2010; 5:213-23; PMID:19946875; http://dx.doi.org/10.1002/biot.200900134
   PubMed Web of Science ®Google Scholar
• Chia MY, Hsiao SH, Chan HT, Do YY, Huang PL, Chang HW, Tsai YC, Lin CM, Pang VF, Jeng CR. The immunogenicity of DNA constructs co-expressing GP5 and M proteins of porcine reproductive and respiratory syndrome virus conjugated by GPGP linker in pigs. Veterinary Microbiol 2010; 146:189-99; PMID:20570063; http://dx.doi.org/10.1016/j.vetmic.2010.05.007
   PubMed Web of Science ®Google Scholar
• Chen X, Zaro JL, Shen WC. Fusion protein linkers: property, design and functionality. Adv Drug Deliv Rev 2013; 65:1357-69; PMID:23026637; http://dx.doi.org/10.1016/j.addr.2012.09.039
   PubMed Web of Science ®Google Scholar
• Radosevic K, Wieland CW, Rodriguez A, Weverling GJ, Mintardjo R, Gillissen G, Vogels R, Skeiky YA, Hone DM, Sadoff JC, et al. Protective immune responses to a recombinant adenovirus type 35 tuberculosis vaccine in two mouse strains: CD4 and CD8 T-cell epitope mapping and role of gamma interferon. Infection and immunity 2007; 75:4105-15; PMID:17526747; http://dx.doi.org/10.1128/IAI.00004-07
   PubMed Web of Science ®Google Scholar
• Skeiky YA, Alderson MR, Ovendale PJ, Guderian JA, Brandt L, Dillon DC, Campos-Neto A, Lobet Y, Dalemans W, Orme IM, et al. Differential immune responses and protective efficacy induced by components of a tuberculosis polyprotein vaccine, Mtb72F, delivered as naked DNA or recombinant protein. J Immunol 2004; 172:7618-28; http://dx.doi.org/10.4049/jimmunol.172.12.7618
   PubMed Web of Science ®Google Scholar
• Irwin SM, Izzo AA, Dow SW, Skeiky YA, Reed SG, Alderson MR, Orme IM. Tracking antigen-specific CD8 T lymphocytes in the lungs of mice vaccinated with the Mtb72F polyprotein. Infect Immun 2005; 73:5809-16; PMID:16113299; http://dx.doi.org/10.1128/IAI.73.9.5809-5816.2005
   PubMed Web of Science ®Google Scholar
• Hel Z, Tsai WP, Tryniszewska E, Nacsa J, Markham PD, Lewis MG, Pavlakis GN, Felber BK, Tartaglia J, Franchini G. Improved vaccine protection from simian AIDS by the addition of nonstructural simian immunodeficiency virus genes. J Immunol 2006; 176:85-96; http://dx.doi.org/10.4049/jimmunol.176.1.85
   PubMed Web of Science ®Google Scholar
• Zhang Y, Sun C, Feng L, Xiao L, Chen L. Enhancement of Gag-specific but reduction of Env- and Pol-specific CD8+ T cell responses by simian immunodeficiency virus nonstructural proteins in mice. AIDS Res hum Retroviruses 2012; 28:374-83; PMID:21736424; http://dx.doi.org/10.1089/aid.2011.0061
   PubMed Web of Science ®Google Scholar
• Beverley PC, Sridhar S, Lalvani A, Tchilian EZ. Harnessing local and systemic immunity for vaccines against tuberculosis. Mucosal Immunol 2014; 7:20-6; PMID:24253104; http://dx.doi.org/10.1038/mi.2013.99
   PubMed Web of Science ®Google Scholar
• Santosuosso M, McCormick S, Zhang X, Zganiacz A, Xing Z. Intranasal boosting with an adenovirus-vectored vaccine markedly enhances protection by parenteral Mycobacterium bovis BCG immunization against pulmonary tuberculosis. Infect Immun 2006; 74:4634-43; PMID:16861651; http://dx.doi.org/10.1128/IAI.00517-06
   PubMed Web of Science ®Google Scholar
• Koblin BA, Casapia M, Morgan C, Qin L, Wang ZM, Defawe OD, Baden L, Goepfert P, Tomaras GD, Montefiori DC, et al. Safety and immunogenicity of an HIV adenoviral vector boost after DNA plasmid vaccine prime by route of administration: a randomized clinical trial. PloS one 2011; 6:e24517; PMID:21931737; http://dx.doi.org/10.1371/journal.pone.0024517
   PubMed Web of Science ®Google Scholar
• Ma C, Li Y, Wang L, Zhao G, Tao X, Tseng CT, Zhou Y, Du L, Jiang S. Intranasal vaccination with recombinant receptor-binding domain of MERS-CoV spike protein induces much stronger local mucosal immune responses than subcutaneous immunization: Implication for designing novel mucosal MERS vaccines. Vaccine 2014; 32:2100-8; PMID:24560617; http://dx.doi.org/10.1016/j.vaccine.2014.02.004
   PubMed Web of Science ®Google Scholar
• Richardson JS, Pillet S, Bello AJ, Kobinger GP. Airway delivery of an adenovirus-based Ebola virus vaccine bypasses existing immunity to homologous adenovirus in nonhuman primates. JVirol 2013; 87:3668-77; PMID:23302894; http://dx.doi.org/10.1128/JVI.02864-12
   PubMed Web of Science ®Google Scholar
• Xiang ZQ, Gao GP, Reyes-Sandoval A, Li Y, Wilson JM, Ertl HC. Oral vaccination of mice with adenoviral vectors is not impaired by preexisting immunity to the vaccine carrier. J Virol 2003; 77:10780-9; PMID:14512528; http://dx.doi.org/10.1128/JVI.77.20.10780-10789.2003
   PubMed Web of Science ®Google Scholar
• Appledorn DM, Aldhamen YA, Godbehere S, Seregin SS, Amalfitano A. Sublingual administration of an adenovirus serotype 5 (Ad5)-based vaccine confirms Toll-like receptor agonist activity in the oral cavity and elicits improved mucosal and systemic cell-mediated responses against HIV antigens despite preexisting Ad5 immunity. Clin Vaccine Immunol 2011; 18:150-60; PMID:21084461; http://dx.doi.org/10.1128/CVI.00341-10
   PubMed Web of Science ®Google Scholar
• Hovav AH. Dendritic cells of the oral mucosa. Mucosal Immunol 2014; 7:27-37; PMID:23757304; http://dx.doi.org/10.1038/mi.2013.42
   PubMed Web of Science ®Google Scholar
• Skeiky YA, Lodes MJ, Guderian JA, Mohamath R, Bement T, Alderson MR, Reed SG. Cloning, expression, and immunological evaluation of two putative secreted serine protease antigens of Mycobacterium tuberculosis. Infect Immun 1999; 67:3998-4007.; PMID:10417166
   PubMed Web of Science ®Google Scholar
• Armitige LY, Jagannath C, Wanger AR, Norris SJ. Disruption of the genes encoding antigen 85A and antigen 85B of Mycobacterium tuberculosis H37Rv: effect on growth in culture and in macrophages. Infect Immun 2000; 68:767-78; PMID:10639445; http://dx.doi.org/10.1128/IAI.68.2.767-778.2000
   PubMed Web of Science ®Google Scholar
• Ahn SS, Jeon BY, Park SJ, Choi DH, Ku SH, Cho SN, Sung YC. Nonlytic Fc-fused IL-7 synergizes with Mtb32 DNA vaccine to enhance antigen-specific T cell responses in a therapeutic model of tuberculosis. Vaccine 2013; 31:2884-90; PMID:23624092; http://dx.doi.org/10.1016/j.vaccine.2013.04.029
   PubMed Web of Science ®Google Scholar
• Romano M, Roupie V, Wang XM, Denis O, Jurion F, Adnet PY, Laali R, Huygen K. Immunogenicity and protective efficacy of tuberculosis DNA vaccines combining mycolyl-transferase Ag85A and phosphate transport receptor PstS-3. Immunology 2006; 118:321-32; PMID:16827893; http://dx.doi.org/10.1111/j.1365-2567.2006.02373.x
   PubMed Web of Science ®Google Scholar
• Tzelepis F, Verway M, Daoud J, Gillard J, Hassani-Ardakani K, Dunn J, Downey J, Gentile ME, Jaworska J, Sanchez AM, et al. Annexin1 regulates DC efferocytosis and cross-presentation during Mycobacterium tuberculosis infection. J Clin Investig 2015; 125:752-68; PMID:25562320; http://dx.doi.org/10.1172/JCI77014
   PubMed Web of Science ®Google Scholar
• Chen CY, Huang D, Wang RC, Shen L, Zeng G, Yao S, Shen Y, Halliday L, Fortman J, McAllister M, et al. A critical role for CD8 T cells in a nonhuman primate model of tuberculosis. PLoS Pathogens 2009; 5:e1000392; PMID:19381260; http://dx.doi.org/10.1371/journal.ppat.1000392
   PubMed Web of Science ®Google Scholar
• Qiu Z, Zhang M, Zhu Y, Zheng F, Lu P, Liu H, Graner MW, Zhou B, Chen X. Multifunctional CD4 T cell responses in patients with active tuberculosis. Sci Rep 2012; 2:216.; PMID:22355730
   PubMed Web of Science ®Google Scholar
• Caccamo N, Guggino G, Joosten SA, Gelsomino G, Di Carlo P, Titone L, Galati D, Bocchino M, Matarese A, Salerno A, et al. Multifunctional CD4(+) T cells correlate with active Mycobacterium tuberculosis infection. Eur J Immunol 2010; 40:2211-20; PMID:20540114; http://dx.doi.org/10.1002/eji.201040455
   PubMed Web of Science ®Google Scholar
• Prezzemolo T, Guggino G, La Manna MP, Di Liberto D, Dieli F, Caccamo N. Functional Signatures of Human CD4 and CD8 T Cell Responses to Mycobacterium tuberculosis. Front Immunol 2014; 5:180; PMID:24795723; http://dx.doi.org/10.3389/fimmu.2014.00180
   PubMed Web of Science ®Google Scholar